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Variation in Physiological Indicators in Bathymodiolus Azoricus

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Variation in Physiological Indicators in Bathymodiolus Azoricus Marine Environmental Research 70 (2010) 264e271 Contents lists available at ScienceDirect Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev Variation in physiological indicators in Bathymodiolus azoricus (Bivalvia: Mytilidae) at the Menez Gwen Mid-Atlantic Ridge deep-sea hydrothermal vent site within a year Virginie Riou a,b,*, Sébastien Duperron c, Sébastien Halary c, Frank Dehairs a, Steven Bouillon a,d, Inès Martins b, Ana Colaço b, Ricardo Serrão Santos b a Department of Analytical and Environmental Chemistry & Earth System Sciences, Vrije Universiteit Brussel, Brussels, Belgium b Department of Oceanography and Fisheries, IMAR-University of Azores, Horta, Portugal c Université Pierre et Marie Curie, UMR 7138 Systématique Adaptation Evolution, Paris, France d Department of Earth and Environmental Sciences, Katholieke Universiteit Leuven, Leuven, Belgium article info abstract Article history: Bathymodiolus azoricus, thriving at Mid-Atlantic Ridge deep vents, benefits from a symbiosis with Received 3 March 2010 methane- and sulphide-oxidising (MOX and SOX) bacteria, and feeds on particulate and dissolved Received in revised form organic matter. To investigate the temporal evolution in their nutrition adult mussels were collected 11 May 2010 from one location at the Menez Gwen vent site (817 m depth) on four occasions between 2006 and 2007 Accepted 15 May 2010 and studied using different techniques, including stable isotope analyses and FISH. Gill and mantle tissues d13C and d15N signatures varied by 2e3& during the year and these variations were linked to Keywords: fluctuations in tissue condition index, C and N contents and SOX/MOX volume ratios as quantified by 3D- Deep ocean Hydrothermal vent FISH. October and January mussels presented a particularly poor condition, possibly related with the Mussel prolonged summer period of low sea-surface primary production and/or with the stress of the transplant Bathymodiolus azoricus to acoustically retrievable cages for the October mussels, and with their reproductive state in January Azores Triple junction mussels, since they were spawning. Our results point to the possibility that May mussels benefited from Food source a pulse of sinking sea-surface plankton material. Results underline the dependency of stable isotopic Stable isotopes signatures on the physiological state of the mussel at the time of collection, and on the type of tissue Condition index analyzed. Tissue analysis Ó 2010 Elsevier Ltd. All rights reserved. 1. Introduction turbulent plume mixing, and tidal cycles render the vent environ- ment highly variable (Lalou et al., 1984; Chevaldonné et al., 1991). The rain of particles derived from sea-surface production is of Such variations may interfere when trying to detect the contribu- great significance in the flux of organic matter into the deep ocean, tion of photosynthesis-derived material on faunal density, distri- and is thought to form a labile food source used for reproductive bution, migration and reproductive cycle at vent sites. growth in many deep-sea fish, echinoderms and bivalves (Tyler, Nevertheless, surface-derived carbon biomarkers (fatty acids) were 1988). However, at deep-sea hydrothermal vents and cold seeps detected in the tissue lipids of Bathymodiolus mytilids showing low (>200 m), the influence of sea-surface photosynthesis-derived numbers of bacterial symbionts, thriving as deep as 2600 m at 13N primary production may appear negligible because of high East Pacific Rise vents (Ben-Mlih et al., 1992). At shallower (650 m) autochthonous chemosynthetic primary production (Tarasov et al., cold seeps on the Louisiana Slope, ‘Bathymodiolus’ childressi was 2005),. In addition, variations in hydrothermal fluid discharge, also observed to supplement its nitrogen requirements by feeding selectively on nitrogen-rich bacterioplankton, as suggested by the variability in nitrogen isotope ratios (Pile and Young, 1999). * Corresponding author at: ANCH-VUB, Pleinlaan 2, 1040 Brussels, Belgium. Tel.: Bathymodiolus mussels are the dominant fauna of numerous þ32 26293970; fax: þ32 26293274. seep and hydrothermal vent ecosystems (Van Dover et al., 2002) E-mail addresses: [email protected] (V. Riou), [email protected] and mussel beds act as habitat or substrate for numerous meio- (S. Duperron), [email protected] (S. Halary), [email protected] (F. Dehairs), [email protected] (S. Bouillon), [email protected] (A. fauna species (Van Dover and Trask, 2000). At the Azores Triple Martins), [email protected] (A. Colaço), [email protected] (R. Serrão Santos). Junction on the Mid-Atlantic Ridge (MAR), the Menez Gwen (MG) 0141-1136/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.marenvres.2010.05.008 V. Riou et al. / Marine Environmental Research 70 (2010) 264e271 265 and Lucky Strike (LS) hydrothermal vent sites ecosystems are and Pond et al. (1998) detected phytoplankton biomarkers in B. dominated by Bathymodiolus azoricus beds (Desbruyères et al., azoricus body lipids, indicating that phytoplankton is accessible for 2000, 2001) which usually are clustering at short distance from the deep hydrothermal vent ecosystem and can be assimilated by the vents (Sarradin et al., 1999; Colaço et al., 1998) but may stretch the vent mussel. Colaço et al. (2009) observed an increase in as far as 3 m away from the hot fluids at the LS Eiffel Tower site phytoplanktonic biomarkers relative to other phospholipid fatty (Cuvelier et al., 2009). Ecological studies of deep-sea hydrothermal acids for MG specimens, which coincided with the autumn bloom. vent habitats are complicated because of the location (mid-ocean) B. azoricus activity at MG thus seems to be influenced, at least to and depth (800e4000 m) of the vent sites. Early biological studies some degree, by surface primary production. on living vent fauna were often restricted to shipboard studies Deposition of phytodetritus to the seafloor is a seasonal, performed on specimens recovered using either a deep-sea possibly pulsed, process and its significance for B. azoricus nutrition submersible or a remote operating vehicle (ROV). These devices can is difficult to assess from annual samplings. In addition, the only operate under good weather conditions, generally during the detection of phytoplankton-derived biomarkers might be masked summer months (from June to September) at the Azores Triple by a changing reproduction-related physiological state of the Junction. The restricted sampling window corresponds to episodes mussel. To resolve these different interfering processes we decided of low surface primary production in the Azores region, where high to investigate the effects of a variable supply of surface-derived photosynthetic production generally occurs between November food on the mussel’s physiology, by collecting vent mussels at 2e3 and May (Colaço et al., 2009). This may induce bias and to under- months intervals covering a complete yearly cycle. Several indica- estimating the impact of photosynthetic production on deep-sea tors can help document the physiological state of the vent mussel. animals including B. azoricus. Time series, or at least sampling of The allometric tissue condition index (TCI: soft tissue dry weight/ a given site several times a year, are necessary to track seasonal shell internal volume) has been recognized as a suitable proxy for phenomena. In this regard, acoustically retrievable cages were physiological condition of the mussel (e.g. Voets et al., 2006). A high developed. Once positioned and filled with surrounding mussels TCI reflects a healthy physiological condition, while a decreased using a ROV these cages are acoustically released and once energy uptake and an increased maintenance cost (for survival) can surfacing, can be recovered from a small research vessel. This result in a low TCI, revealing reduced growth and/or reproduction technique enables faster, year-round and ROV-independent mussel (De Coen and Janssen, 2003). A time-course examination of TCI collection (Fig. 1, Dixon et al., 2001). should thus inform on the health condition of the mussels, as At known northern MAR vent sites, B. azoricus occurs at possibly influenced by their translocation and adaptation to the different depths ranging from 817 to 3080 m (Menez Gwen -MG-, cage environment, variability in food supply and spawning events. Lucky Strike, Rainbow and Broken Spur, Desbruyères et al., 2000; Since tissue C:N ratio can be affected by the storage or use of O’Mullan et al., 2001). B. azoricus possesses a dual endosymbiosis reserves, it also represents a powerful indicator of the animal’s with methane- and sulphide-oxidising Gammaproteobacteria physiological condition (Okumura et al., 2002). Indeed, proteins (MOX and SOX, respectively, Fiala-Médioni et al., 2002; Duperron and nucleic acids are enriched in nitrogen, compared to the et al., 2006) located in specialised cells (bacteriocytes) of the gill nitrogen-poor lipids and carbohydrates (e.g. glycogen), also used as epithelial tissue. These symbionts ensure (at least part of) the host storage compounds. The catabolism of lipids and carbohydrates nutrition (Fisher, 1990; Martins et al., 2008; Riou et al., 2008) with will lead to a decrease in C:N ratio, and proteins will only be used as assimilation of particulate and dissolved organic matter demon- an internal energy source when glycogen reserves are exhausted, strated to represent a further nutritional mode to B. azoricus (Riou resulting in increased
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